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Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes

BACKGROUND: Campylobacter jejuni is commonly found in the gastrointestinal tract of many food-animals including sheep without causing visible clinical symptoms of disease. However, C. jejuni has been implicated in ovine abortion cases worldwide. Specifically, in the USA, the C. jejuni sheep abortion...

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Autores principales: Sanad, Yasser M, Jung, Kwonil, Kashoma, Isaac, Zhang, Xiaoli, Kassem, Issmat I, Saif, Yehia M, Rajashekara, Gireesh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4262353/
https://www.ncbi.nlm.nih.gov/pubmed/25420712
http://dx.doi.org/10.1186/s12917-014-0274-8
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author Sanad, Yasser M
Jung, Kwonil
Kashoma, Isaac
Zhang, Xiaoli
Kassem, Issmat I
Saif, Yehia M
Rajashekara, Gireesh
author_facet Sanad, Yasser M
Jung, Kwonil
Kashoma, Isaac
Zhang, Xiaoli
Kassem, Issmat I
Saif, Yehia M
Rajashekara, Gireesh
author_sort Sanad, Yasser M
collection PubMed
description BACKGROUND: Campylobacter jejuni is commonly found in the gastrointestinal tract of many food-animals including sheep without causing visible clinical symptoms of disease. However, C. jejuni has been implicated in ovine abortion cases worldwide. Specifically, in the USA, the C. jejuni sheep abortion (SA) clone has been increasingly associated with sheep abortion. In vivo studies in sheep (the natural host) are needed to better characterize the virulence potential and pathogenesis of this clone. RESULTS: Pregnant ewes intravenously (IV) or orally inoculated with ovine or bovine abortion-associated C. jejuni SA clones exhibited partial or complete uterine prolapse with retained placenta, and abortion or stillbirth, whereas delivery of healthy lambs occurred in pregnant ewes inoculated with C. jejuni 81–176 or in the uninfected group. In sheep inoculated with the SA clone, histopathological lesions including suppurative necrotizing placentitis and/or endometritis coincided with: 1) increased apoptotic death of trophoblasts, 2) increased expression of the host genes (e.g. genes encoding interleukin IL-6 and IL-15) related to cellular necrosis and pro-inflammatory responses in uterus, and 3) decreased expression of the genes encoding GATA binding protein 6, chordin, and insulin-like 3 (INSL3) that account for embryonic development in uterus. Immunohistochemistry revealed localization of bacterial antigens in trophoblasts lining the chorioallantoic membrane of ewes inoculated with the C. jejuni SA clone. CONCLUSIONS: The results showed that C. jejuni SA clones are capable of causing abortion or stillbirth in experimentally infected sheep. Furthermore, down- or up-regulation of specific genes in the uterus of infected pregnant ewes might implicate host genes in facilitating the disease progression. Since the C. jejuni SA strains share genotypic similarities with clones that have been isolated from human clinical cases of gastroenteritis, these strains might represent a potential public health risk. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12917-014-0274-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-42623532014-12-11 Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes Sanad, Yasser M Jung, Kwonil Kashoma, Isaac Zhang, Xiaoli Kassem, Issmat I Saif, Yehia M Rajashekara, Gireesh BMC Vet Res Research Article BACKGROUND: Campylobacter jejuni is commonly found in the gastrointestinal tract of many food-animals including sheep without causing visible clinical symptoms of disease. However, C. jejuni has been implicated in ovine abortion cases worldwide. Specifically, in the USA, the C. jejuni sheep abortion (SA) clone has been increasingly associated with sheep abortion. In vivo studies in sheep (the natural host) are needed to better characterize the virulence potential and pathogenesis of this clone. RESULTS: Pregnant ewes intravenously (IV) or orally inoculated with ovine or bovine abortion-associated C. jejuni SA clones exhibited partial or complete uterine prolapse with retained placenta, and abortion or stillbirth, whereas delivery of healthy lambs occurred in pregnant ewes inoculated with C. jejuni 81–176 or in the uninfected group. In sheep inoculated with the SA clone, histopathological lesions including suppurative necrotizing placentitis and/or endometritis coincided with: 1) increased apoptotic death of trophoblasts, 2) increased expression of the host genes (e.g. genes encoding interleukin IL-6 and IL-15) related to cellular necrosis and pro-inflammatory responses in uterus, and 3) decreased expression of the genes encoding GATA binding protein 6, chordin, and insulin-like 3 (INSL3) that account for embryonic development in uterus. Immunohistochemistry revealed localization of bacterial antigens in trophoblasts lining the chorioallantoic membrane of ewes inoculated with the C. jejuni SA clone. CONCLUSIONS: The results showed that C. jejuni SA clones are capable of causing abortion or stillbirth in experimentally infected sheep. Furthermore, down- or up-regulation of specific genes in the uterus of infected pregnant ewes might implicate host genes in facilitating the disease progression. Since the C. jejuni SA strains share genotypic similarities with clones that have been isolated from human clinical cases of gastroenteritis, these strains might represent a potential public health risk. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12917-014-0274-8) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-25 /pmc/articles/PMC4262353/ /pubmed/25420712 http://dx.doi.org/10.1186/s12917-014-0274-8 Text en © Sanad et al.; licensee BioMed Central Ltd. 2014 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sanad, Yasser M
Jung, Kwonil
Kashoma, Isaac
Zhang, Xiaoli
Kassem, Issmat I
Saif, Yehia M
Rajashekara, Gireesh
Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes
title Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes
title_full Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes
title_fullStr Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes
title_full_unstemmed Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes
title_short Insights into potential pathogenesis mechanisms associated with Campylobacter jejuni-induced abortion in ewes
title_sort insights into potential pathogenesis mechanisms associated with campylobacter jejuni-induced abortion in ewes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4262353/
https://www.ncbi.nlm.nih.gov/pubmed/25420712
http://dx.doi.org/10.1186/s12917-014-0274-8
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